XB-ART-56277
PLoS One
January 1, 2019;
14
(9):
e0222106.
Action spectrum for photoperiodic control of thyroid-stimulating hormone in Japanese quail (Coturnix japonica).
Nakane Y
,
Shinomiya A
,
Ota W
,
Ikegami K
,
Shimmura T
,
Higashi SI
,
Kamei Y
,
Yoshimura T
.
Abstract
At higher latitudes, vertebrates exhibit a seasonal cycle of reproduction in response to changes in day-length, referred to as photoperiodism. Extended day-length induces
thyroid-stimulating hormone in the pars tuberalis of the
pituitary gland. This hormone triggers the local activation of
thyroid hormone in the mediobasal
hypothalamus and eventually induces gonadal development. In avian species, light information associated with day-length is detected through photoreceptors located in
deep-
brain regions. Within these regions, the expressions of multiple photoreceptive molecules, opsins, have been observed. However, even though the Japanese quail is an excellent model for photoperiodism because of its robust and significant seasonal responses in reproduction, a comprehensive understanding of photoreceptors in the quail
brain remains undeveloped. In this study, we initially analyzed an action spectrum using photoperiodically induced expression of the beta subunit genes of
thyroid-stimulating hormone in quail. Among seven wavelengths examined, we detected maximum sensitivity of the action spectrum at 500 nm. The low value for goodness of fit in the alignment with a template of retinal1-based photopigment, assuming a spectrum associated with a single opsin, proposed the possible involvement of multiple opsins rather than a single opsin. Analysis of gene expression in the septal region and
hypothalamus, regions hypothesized to be photosensitive in quail, revealed mRNA expression of a mammal-like
melanopsin in the infundibular
nucleus within the mediobasal
hypothalamus. However, no significant diurnal changes were observed for genes in the infundibular
nucleus. Xenopus-like
melanopsin, a further isoform of
melanopsin in birds, was detected in neither the septal region nor the infundibular
nucleus. These results suggest that the mammal-like
melanopsin expressed in the infundibular
nucleus within the mediobasal
hypothalamus could be candidate
deep-
brain photoreceptive molecule in Japanese quail. Investigation of the functional involvement of mammal-like
melanopsin-expressing cells in photoperiodism will be required for further conclusions.
PubMed ID:
31509560
PMC ID:
PMC6738599
Article link:
PLoS One
Species referenced:
Xenopus laevis
Genes referenced:
opn4
ptch1
tshb
XB5957215 [provisional]
Article Images:
[+] show captions
|
Fig 1. Spectral characteristics of the transmittance of various wavelengths of light reaching the quail hypothalamus.Relative transmittance pattern (T/Tmax) of various wavelengths of light penetrating the feathers, skin, skull, and brain tissue are indicated. Each point represents the mean ±SEM (n = 3).
|
|
Fig 2. The action spectrum using the photoperiodically induced beta subunit of thyroid-stimulating hormone.(A) Schedule for light exposure and sampling. Eye-patched birds lacking pineal organ and maintained under short-day conditions (6 h:18 h light/dark cycle: 6L18D) were given a long-day stimulus by extending the 6-h light period by 10 h with light of seven different wavelengths. (B) The effects of four intensities of light at each wavelength on the expressions of photoperiodically induced mRNA encoding the beta subunit of thyroid-stimulating hormone (TSHB) in the pars tuberalis of the pituitary gland were evaluated by in situ hybridization. (C) Each expression level of TSHB was plotted to examine the dependence of photoperiodic responses on irradiance with monochromatic lights of seven different wavelengths. Each light intensity (photons m2 s-1) was adjusted to the light intensity at the deep-brain region level using the percentage of T/Tmax. Each point represents the mean ± SEM (n = 4). (D) The action spectrum for photoperiodic TSHB induction. The half-saturation constant (EC50) derived from sigmoidal fits of the light intensity–response curves were plotted against wavelength. The action spectrum was then fitted with a curve for retinal1-based photopigment using the least-squares method. Peak sensitivity was approximately 479.2 nm with a low value for the goodness of fit (adjusted R2 = -0.938).
|
|
Fig 3. Expressions of mammal-like and Xenopus-like melanopsins in the quail brain.(A) The expression of mRNA encoding mammal-like melanopsin (OPN4m) was detected in the infundibular nucleus (IN) within the mediobasal hypothalamus (MBH) (arrowheads in the lower row); however, OPN4m was not detected in the septal region. Faint expression of Xenopus-like melanopsin (OPN4x) mRNA was detected in the septal region (arrowheads in the upper raw) but was not detected in the MBH. (B) Expression analysis of both melanopsins based on high-sensitivity in situ hybridization revealed the expression of OPN4m in the IN (arrowheads in a high-magnification image). (C) The JTK_CYCLE algorithm revealed a pattern of OPN4m expression in the IN that lacked a distinctive periodicity (adjusted p-value: 1.0, Benjamini–Hochberg q-value: 1.0, period: 20, Phase 12). Each point represents the mean ± SEM (n = 3). CO: optic chiasm, IN: infundibular nucleus, LS: lateral septum, LV: lateral ventricle, ME: median eminence, PVO: paraventricular organ, 3V: third ventricle.
|
References [+] :
Altimus,
Rod photoreceptors drive circadian photoentrainment across a wide range of light intensities.
2010,
Pubmed
Altimus,
Rod photoreceptors drive circadian photoentrainment across a wide range of light intensities.
2010,
Pubmed
Bailey,
Melanopsin expression in the chick retina and pineal gland.
2005,
Pubmed
Bellingham,
Evolution of melanopsin photoreceptors: discovery and characterization of a new melanopsin in nonmammalian vertebrates.
2006,
Pubmed
,
Xenbase
Chaurasia,
Molecular cloning, localization and circadian expression of chicken melanopsin (Opn4): differential regulation of expression in pineal and retinal cell types.
2005,
Pubmed
,
Xenbase
Davies,
Vertebrate ancient opsin photopigment spectra and the avian photoperiodic response.
2012,
Pubmed
Foster,
Immunocytochemical markers revealing retinal and pineal but not hypothalamic photoreceptor systems in the Japanese quail.
1987,
Pubmed
Foster,
Rhodopsin-like sensitivity of extra-retinal photoreceptors mediating the photoperiodic response in quail.
1985,
Pubmed
Franzoni,
A Golgi study on the neuronal morphology in the hypothalamus of the Japanese quail (Coturnix coturnix japonica). I. Tuberal and mammillary regions.
1984,
Pubmed
García-Fernández,
The hypothalamic photoreceptors regulating seasonal reproduction in birds: a prime role for VA opsin.
2016,
Pubmed
Glass,
Sites and action spectra for encephalic photoreception in the Japanese quail.
1981,
Pubmed
Haida,
Photoperiodic response of serotonin- and galanin-immunoreactive neurons of the paraventricular organ and infundibular nucleus in Japanese quail, Coturnix coturnix japonica.
2004,
Pubmed
Halford,
VA opsin-based photoreceptors in the hypothalamus of birds.
2009,
Pubmed
Hanon,
Ancestral TSH mechanism signals summer in a photoperiodic mammal.
2008,
Pubmed
Hattar,
Melanopsin and rod-cone photoreceptive systems account for all major accessory visual functions in mice.
2003,
Pubmed
Hughes,
JTK_CYCLE: an efficient nonparametric algorithm for detecting rhythmic components in genome-scale data sets.
2011,
Pubmed
Kang,
Melanopsin expression in dopamine-melatonin neurons of the premammillary nucleus of the hypothalamus and seasonal reproduction in birds.
2011,
Pubmed
Kato,
Two Opsin 3-Related Proteins in the Chicken Retina and Brain: A TMT-Type Opsin 3 Is a Blue-Light Sensor in Retinal Horizontal Cells, Hypothalamus, and Cerebellum.
2017,
Pubmed
Kojima,
Vertebrate ancient-long opsin: a green-sensitive photoreceptive molecule present in zebrafish deep brain and retinal horizontal cells.
2000,
Pubmed
Kojima,
UV-sensitive photoreceptor protein OPN5 in humans and mice.
2012,
Pubmed
Lamb,
Photoreceptor spectral sensitivities: common shape in the long-wavelength region.
1996,
Pubmed
Menaker,
Extraretinal light perception in the sparrow. 3. The eyes do not participate in photoperiodic photoreception.
1970,
Pubmed
Moore,
The premammillary nucleus of the hypothalamus is not necessary for photoperiodic timekeeping in female turkeys (Meleagris gallopavo).
2018,
Pubmed
Nakane,
A mammalian neural tissue opsin (Opsin 5) is a deep brain photoreceptor in birds.
2010,
Pubmed
,
Xenbase
Nakane,
The saccus vasculosus of fish is a sensor of seasonal changes in day length.
2013,
Pubmed
Nakane,
Intrinsic photosensitivity of a deep brain photoreceptor.
2015,
Pubmed
Nakao,
Thyrotrophin in the pars tuberalis triggers photoperiodic response.
2008,
Pubmed
Oliver,
Plasma testosterone and LH levels in male quail bearing hypothalamic lesions or radioluminous implants.
1979,
Pubmed
Ono,
Involvement of thyrotropin in photoperiodic signal transduction in mice.
2009,
Pubmed
Philp,
A novel rod-like opsin isolated from the extra-retinal photoreceptors of teleost fish.
2000,
Pubmed
Shimmura,
Dynamic plasticity in phototransduction regulates seasonal changes in color perception.
2017,
Pubmed
Silver,
Coexpression of opsin- and VIP-like-immunoreactivity in CSF-contacting neurons of the avian brain.
1988,
Pubmed
Siopes,
Extraocular modification of photoreception in intact and pinealectomized coturnix.
1975,
Pubmed
Soni,
A novel and ancient vertebrate opsin.
1997,
Pubmed
Soni,
Novel retinal photoreceptors.
1998,
Pubmed
Torii,
Two isoforms of chicken melanopsins show blue light sensitivity.
2008,
Pubmed
Vigh-Teichmann,
Comparison of the pineal complex, retina and cerebrospinal fluid contacting neurons by immunocytochemical antirhodopsin reaction.
1981,
Pubmed
Wada,
Phototransduction molecules in the pigeon deep brain.
2000,
Pubmed
Wang,
RNAscope: a novel in situ RNA analysis platform for formalin-fixed, paraffin-embedded tissues.
2012,
Pubmed
Yamamura,
Seasonal morphological changes in the neuro-glial interaction between gonadotropin-releasing hormone nerve terminals and glial endfeet in Japanese quail.
2004,
Pubmed
Yamashita,
Opn5 is a UV-sensitive bistable pigment that couples with Gi subtype of G protein.
2011,
Pubmed
Yasuo,
Differential response of type 2 deiodinase gene expression to photoperiod between photoperiodic Fischer 344 and nonphotoperiodic Wistar rats.
2007,
Pubmed
Yokoyama,
The sites of encephalic photoreception in phosoperiodic induction of the growth of the testes in the white-crowned sparrow, Zonotrichia leucophrys gambelii.
1978,
Pubmed
Yoshimura,
Molecular analysis of avian circadian clock genes.
2000,
Pubmed
Yoshimura,
Light-induced hormone conversion of T4 to T3 regulates photoperiodic response of gonads in birds.
2003,
Pubmed
Yoshimura,
Spectral sensitivity of photoreceptors mediating phase-shifts of circadian rhythms in retinally degenerate CBA/J (rd/rd) and normal CBA/N (+/+)mice.
1996,
Pubmed
Zhao,
Daily, circadian and seasonal changes of rhodopsin-like encephalic photoreceptor and its involvement in mediating photoperiodic responses of Gambel's white-crowned Sparrow, Zonotrichia leucophrys gambelii.
2019,
Pubmed
